Functional host-specific adaptation of the intestinal microbiome in hominids

Fine-scale knowledge of the changes in composition and function of the human gut microbiome compared that of our closest relatives is critical for understanding the evolutionary processes underlying its developmental trajectory. To infer taxonomic and functional changes in the gut microbiome across hominids at different timescales, we perform high-resolution metagenomic-based analyzes of the fecal microbiome from over two hundred samples including diverse human populations, as well as wild-living chimpanzees, bonobos, and gorillas. We find human-associated taxa depleted within non-human apes and patterns of host-specific gut microbiota, suggesting the widespread acquisition of novel microbial clades along the evolutionary divergence of hosts. In contrast, we reveal multiple lines of evidence for a pervasive loss of diversity in human populations in correlation with a high Human Development Index, including evolutionarily conserved clades. Similarly, patterns of co-phylogeny between microbes and hosts are found to be disrupted in humans. Together with identifying individual microbial taxa and functional adaptations that correlate to host phylogeny, these findings offer insights into specific candidates playing a role in the diverging trajectories of the gut microbiome of hominids. We find that repeated horizontal gene transfer and gene loss, as well as the adaptation to transient microaerobic conditions appear to have played a role in the evolution of the human gut microbiome.

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Study description
Research sample version 207v2, eggNOG database (v5.0) We did not stratify or correct for sex or gender effects in the analysis.Our analyses focus on the comparison of gut metagenomes from either distinct hominid species or between human subgroups from populations with differences in human development index.The effects of sex and/or gender are negligible in this context.
In our analysis we included fecal samples from humans from Germany and two rural locations in Africa (Côte d'Ivoire and Democratic Republic of the Congo).These samples represent a spectrum of human populations with differences in Human Development Index and associated factors.We require information from authors about some types of materials, experimental systems and methods used in many studies.Here, indicate whether each material, system or method listed is relevant to your study.If you are not sure if a list item applies to your research, read the appropriate section before selecting a response.
Sample sizes were chosen to meet a common ground between broadness of included hosts, statistical power and available funds.Many of the included host species / groups were never included in fecal metagenomic studies before, thus the choice of 10-12 individuals per group was chosen appropriate.
Samples from wild-living African great apes were collected from habituated groups after defecation.Data on feces-to-individual mappings were recorded in the field and later recorded electronically.12 samples of each African great ape subgroup were subjected to shotgun metagenomic sequencing, except for the P.t.verus group for which 55 samples were included.Four G. b. beringei, one G.g. gorilla and one P.t.troglodytes sample failed sequencing, not producing any data.Further samples with less than 1 Million mapped reads were removed from further analyses.This resulted in the removal of samples from the analysis for the groups G.b. beringei (n=1), G.g. gorilla (nGAB=5, nCG=1), P.t.troglodytes (nGAB=4), P.t.schweinfurthii (n=1) and humans from CIV (n=1)

Single
Single-timepoint data was used for all included individuals.By collecting samples from multiple individuals from each subgroup we can confidently identify group-specific robust signatures in the composition of the fecal microbiota.All information ond data, software and code used for the processing and dowstream analysis are provided in public repositories on the projects github page for reproducibility.
Not applicable as sampling was performed from populations and not treatments were applied Not applicable as sampling was performed from populations and not treatments were applied Samples were collected from multiple locations including cities, rural villages and rain forests.No disturbances affecting the studies results were recorded -timepoint data was used for all included individuals.Sampling periods: Gorilla beringei beringei from Bwindi: 2011; Gorilla gorilla gorilla from Loango: 2015-2016; Pan paniscus from Kokolopori: 2017; Pan troglodytes troglodytes from Loango: 2016-2017; Pan troglodytes schweinfurthii from Budongo: 2004-2008: Pan troglodytes verus from Taï National Park: 2001-2014; humans in Democratic Republic of Congo: 2011; humans in Côte d'Ivoire: 2011; humans in Germany: 2012-2014 Sampling periods: Gorilla beringei beringei from Bwindi: 2011; Gorilla gorilla gorilla from Loango: 2015-2016; Pan paniscus from Kokolopori: 2017; Pan troglodytes troglodytes from Loango: 2016-2017; Pan troglodytes schweinfurthii from Budongo: 2004-2008: Pan troglodytes verus from Taï National Park: 2001-2014; humans in Democratic Republic of Congo: 2011; humans in Côte d'Ivoire: 2011; humans in Germany: 2012-2014 Bwindi National Park, Uganda; Kokolopori Bonobo Reserve, Democratic Republic of the Congo; Loango National Park, Gabon; Taï National Park, Côte d'Ivoire Bwindi-The mountain gorilla survey was conducted by the Uganda Wildlife Authority, l'Institut Congolais pour la Conservation de la Nature, the Rwanda Development Board, the International Gorilla Conservation Programme, the Max Planck Institute for Evolutionary Anthropology, Conservation Through Public Health, the Mountain Gorilla Veterinary Project, the Institute for Tropical Forest Conservation, and The Dian Fossey Gorilla Fund and was conducted in compliance with the regulations of and permission of the Uganda National Council for Science and Technology and the Uganda Wildlife Authority; Kokolopori-permission was granted through the Ministere de Recherche Scientifique et Technologie, Democratic Republic of the Congo, and work was supported by the Vie Sauvage, the Bonobo Conservation Initiative; Loango-permission was granted by the Agence Nationale des Parcs Nationaux, the Centre National de la Recherche Scientifique et Technique of Gabon; Taï National Park-permission was granted by the Ministère de l'Enseignement Supérieur et de la Recherche Scientifique, the Ministère des Eaux et Fôrets in Côte d'Ivoire, and the Office Ivoirien des Parcs et Réserves, and work was supported by the Centre Suisse de Recherches Scientifiques en Côte d'Ivoire and the staff members of the Taï Chimpanzee Project.
Due to the rather low sample sizes (24 GER, 24 DK, 12 CIV, 12 DRC), comparisons were made only based on geographic location (EUR vs. AFR) without further stratifying / subgrouping the samples.
), the Ivorian ethics commission (Comité national d'éthique et de la recherche[CNER], permit number 101 10/MSHP/CNER/P) and the Congolese ethics commission (Comité d'Éthique, Ministère de l'Enseignement Supérieur et Universiaire, permit number ESO/CE/018/11).All procedures performed in studies involving human participants were in accordance with the ethical standards of the institutional and/or national research committee and with the 1975 Helsinki declaration and its later amendments or comparable ethical standards.Sampling of wild-living great apes and human populations in Africa were granted by: BwindiImpenetrableForest National Park, Uganda (Gorilla beringei beringi, Pan troglodytes schweinfurthii): the Uganda National Council for Science and Technology and the Uganda Wildlife Authority; Kokolopori Bonobo Reserve and Bandundu region, Democratic Republic of the Congo (Pan paniscus, Human): the Ministere de Recherche Scientifique et Technologie, Democratic Republic of the Congo; Loango National Park, Gabon (Gorilla gorilla gorilla, Pan troglodytes troglodytes): the Agence Nationale des Parcs Nationaux, the Centre National de la Recherche Scientifique et Technique of Gabon; Taï National Park and region, Côte d'Ivoire (Pan troglodytes verus, Human): the Ministère de l'Enseignement Supérieur et de la Recherche Scientifique, the Ministère des Eaux et Fôrets in Côte d'Ivoire, and the Office Ivoirien des Parcs et Réserves.Local researchers from CIV and DRC contributing to the conducted research and fulfilling the authorship criteria were included as co-authors.fromhumans (n=24) from Denmark (DK) were included.The trial was purely observational, no treatments were performed.All samples included were from individual humans and great apes.Host were chosen based on the availability from participating research institutions and aimed to cover a broad range of African great ape (sub-species) including two gorilla subspecies (Gorilla gorilla gorilla, Gabon (GAB), n=8; Gorilla beringei beringei, Uganda (UGA), n=11), three chimpanzee subspecies (Pan troglodytes verus, CIV, n=55; P.t.troglodytes, GAB, n=11; P.t.schweinfurthii, UGA, n=12), and bonobos (Pan paniscus, DRC, n=12).Great ape groups were habituated and not actively interacted with.